Knowl. Manag. Aquat. Ecosyst. 2017, 418, 25 Knowledge & © R. Rocaspana and E. Aparicio, Published by EDP Sciences 2017 Management of Aquatic DOI: 10.1051/kmae/2017017 Ecosystems www.kmae-journal.org Journal fully supported by Onema

SHORT COMMUNICATION

Population trends and current status of the endangered Pyrenean hispaniolensis in the Spanish part of the Garonne drainage

Rafel Rocaspana1 and Enric Aparicio2,* 1 Gesna Estudis Ambientals, Prat de la Riba 51, 25240 Linyola, , 2 GRECO, Institute of Aquatic Ecology, University of Girona, 17071 Girona, Catalonia, Spain

Abstract – The status of Pyrenean sculpin was assessed in the Spanish part of the Garonne drainage on the basis of its distribution and abundance from 2001 to 2016. Population trends showed a progressive reduction in range extension and density, exacerbated by a severe spate occurred in 2013. However, C. hispaniolensis was resilient to this natural disturbance by compensating for mortality with increasing recruitment. Both occurrence and density of Pyrenean sculpin showed a positive correlation with coarse substrates. Riverine habitat deterioration, mainly channelization, presence of dams and flow regulation are the main factors threatening sculpin populations. Several management measures are proposed.

Keywords: abundance / catastrophic spate / conservation measures / Cottus hispaniolensis / Garonne

Résumé – Tendances et état actuel de la population du chabot pyrénéen menacé Cottus hispaniolensis dans la partie espagnole du bassin de la Garonne. Le statut du chabot pyrénéen Cottus hispaniolensis a été évalué dans la partie espagnole du bassin de la Garonne sur la base des données de distribution et d’abondance au cours de la période 2001-2016. Les tendances de la population ont montré un déclin progressif de l’extension de répartition et de la densité, exacerbé par une crue sévère survenue en 2013. Cependant, C. hispaniolensis a montré une résilience à ce type de perturbation naturelle en compensant la mortalité par un recrutement accru. L’occurrence et la densité du chabot pyrénéen ont montré une corrélation positive avec les substrats grossiers. La détérioration des habitats rivulaires, principalement la canalisation des cours d’eau, la présence de barrages et la régulation des débits, sont les principaux facteurs potentiels qui menacent les populations de chabots. Plusieurs actions de gestion sont proposées.

Mots clés : abondance / crue catastrophique / Mesures de conservation / Distribution

The (Cottus sp., , ) are and brown trutta L. 1758, and the introduced small benthic-dwelling freshwater fish species that occur minnow Phoxinus sp. and Alpine charr umbla mainly in cold, well-oxygenated mountain streams and (L. 1758) are found in a few reservoirs and high mountain lakes (Tomlinson and Perrow, 2003). In Spain, two native sculpin (Aparicio, 2015). Pyrenean sculpin historically occurred in species with a very restricted distribution are found (Doadrio continuous populations located in the main course of the et al., 2011): Adour sculpin (Freyhof, Kottelat Garonne and the lower parts of some tributaries and Nolte, 2005) and Pyrenean sculpin Cottus hispaniolensis (de Sostoa et al., 1990; Doadrio et al., 2011). These Bǎcescu and Bǎcescu-Meşter, 1964. The latter is endemic to populations are declining in relation to historical information, the Garonne River basin (south west and northern but available quantitative data is scarce (Doadrio et al., 2011; Spain) restricted to the southern (upper) part of the drainage in Sousa-Santos et al., 2014). Pyrenean sculpin is currently listed the (Freyhof et al., 2005). as Critically Endangered in the Spanish and Catalan Red Lists The source of the Garonne River is located in the Val of Threatened Species (Doadrio et al., 2011; Aparicio et al., d’Aran (Catalonia, Spain), and flows for ca. 40 km before 2016) and, as Cottus gobio (former synonym), is also included entering to France. assemblages in the Spanish part of the in Annex II of the European Habitats Directive 92/43/EEC. In drainage are almost exclusively composed of Pyrenean sculpin France, there is no available information on its status, and is included as Data Deficient in the French Red List (Keith et al., * Corresponding author: [email protected] 2011).

This is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material. R. Rocaspana and E. Aparicio: Knowl. Manag. Aquat. Ecosyst. 2017, 418, 25

Fig. 1. Map of the Garonne drainage in the Val d’Aran (Catalonia, Spain) and location of the sampling sites (see codes in Tab. 1) showing the distribution area of Pyrenean sculpin Cottus hispaniolensis:(○) indicates sites with fish information data and (●) indicates sites where C. hispaniolensis is positively recorded. Physical barriers (weirs and dams) are marked as lines perpendicular to the river.

In June 2013, heavy rain combined with snow melting Fish was sampled from 15 sites during summer and early caused a severe spate in the Garonne River and its tributaries autumn base flow conditions, from 2001 to 2016. Sampling (the estimated return period is 50 years). According to data sites (80–200 m in length) were selected in relation to the from the Bossòst gauging station (42°470100 N; 0°4103200 E), historical range of Pyrenean sculpin, i.e. the main course of flow discharge during the spate exceed 300 m3 s1, whereas the the Garonne River and the lower parts of its main tributaries mean discharge for the 1966–2013 period was 17.3 m3 s1 (Fig. 1). Fish were captured by two pass electrofishing (Ebro Water Authority; http://www.chebro.es/). The cata- (pulsed DC). All captured fish were anaesthetized with clove strophic spate induced dramatic changes in the streams oil, identified to species level, counted, measured (fork length morphology and its consequences produced an additional (FL), mm), weighed (g) and released at the same location concern about the fate of Pyrenean sculpin. The aim of this after recovery. Population sizes (N) of both Pyrenean sculpin ¼ 2ð Þ1 study was to summarize existing data on the distribution and and were estimated as N C1 C1 C2 , abundance of Pyrenean sculpin in the Spanish part of the where C1 is the number of fish captured in the first sample and Garonne drainage, and to provide information on the effects of C2 is the number of individuals caught in the second event; 1 the spate of 2013 on their populations. probability of capture was calculated as p =(C1C2)(C1)

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Table 1. Mean density, density range and percentage of occurrence of Pyrenean sculpin Cottus hispaniolensis in the sampling sites during the period 2001–2016. Information of sampling sites subjected to flow regulation is also included.

River Code Regulated N Occurrence (%) Mean density ± SD (ind. ha1) Range (ind. ha1)

Garonne 1 No 5 83 167.8 ± 167.4 0–416.7 Garonne 2 Yes 5 67 41.9 ± 57.1 0–138.9 Garonne 3 Yes 5 100 130.8 ± 111.6 24.4–258.1 Garonne 4 Yes 5 67 49.3 ± 57.3 0–133.3 Garonne 5 Yes 5 67 49.1 ± 54.7 0–111.1 Garonne 6 Yes 5 33 8.9 ± 19.9 0–44.4 Garonne 7 Yes 4 60 14.9 ± 27.1 0–55.6 Ruda 8 No 50 –– Unhola 9 No 50 –– Aiguamòg 10 No 4 60 64.4 ± 106.5 0–222.2 Valarties 11 No 50 –– Nere 12 No 4 60 107.8 ± 135.5 0–281.1 Varradòs 13 No 5 100 288.5 ± 146.2 121.0–500.0 Joeu 14 No 5 83 306.1 ± 388.1 0–925.9 Toran 15 Yes 50 ––

(Seber and Le Cren, 1967). Fish density (individuals ha1) length-frequency distribution data (Fig. 3) showed a simplified was calculated by dividing estimated number of fish by the structure, dominated by fish from 85 to 135 mm FL, and the 0þ area sampled. Because different sampling efforts were class (<50 mm) was very scarce. The spate occurred in sculpin performed from 2001 to 2013 and not all sites were sampled spawningtime(spring)andcoulddamage the nestsorflush down annually, samples were time pooled as following: 2001–2005, the newly hatched fry (Natsumeda, 2005). In 2015, the 0þ class 2006–2012, 2014, 2015 and 2016. After fish sampling, the was also scarce probably because of a small stock of mature streambed substrate was visually estimated (percentage individuals in the reproductive season. In 2016, 3 years after the composition) and classified according to a modified Went- spate, length frequency distribution showed a substantial worth scale: boulder (particle size >256 mm), cobble (>64– increase in the 0þ class (53.6% of the individuals). These 256 mm), pebble (>16–64 mm), gravel (>2–16 mm), sand results suggest that Pyrenean sculpin populations are resilient to (0.1–2mm)andsilt(<0.1 mm). Percent of the sampled reach severe spates, compensating for mortality with increasing that is pool, riffle, or run habitat was also recorded. Stepwise recruitment in the following years. multiple linear regression was used to test the effect of habitat The linear regression (stepwise procedure, P < 0.05) (substrate composition, channel units, and flow regulation) revealed significant relationships of both sculpin density and biotic (mean brown trout density) predictors on mean and occurrence with substrate composition, explaining the sculpin density and occurrence. The significance level for 78% of the difference in mean density and 72% of the predictor variables was 0.05. Fish densities were log10(x þ 1) difference in percentage of occurrence. Percent boulders, transformed and percentage data were normalized using an cobble and sand were positively related, with the first two arcsine square-root transformation. having the strongest effect (Tab. 2); and the proportion of Results showed that Pyrenean sculpin populations in the pools, runs and riffles, stream regulation, and brown trout Spanish part of the Garonne drainage were scarce (Tab. 1), density was not significantly related to sculpin density and confined to localized areas of the streams, and most of them occurrence. Our results are similar to those showed by Legalle isolated due to the presence of artificial barriers (Fig. 1). et al. (2005a, 2005b) for sculpin populations in the French part Brown trout coexisted with Pyrenean sculpin, being dominant of the Garonne drainage, where fish selected areas of coarse in density (brown trout mean density ± SD = 1988 ± 1718 ind. substrate where water velocity is weakened and sand ha1; range: 63–7570 ind. ha1). The proportion of positive accumulates. detections (namely range extension) of Pyrenean sculpin was Because Pyrenean sculpin populations currently exhibit progressively reduced from the 69.2% in the 2001–2005 period lower densities with a reduced range and mostly fragmented, to the 46.7% in 2016. Mean densities also decreased over this maintaining the status of Critically Endangered is advised. Our period (Fig. 2). The natural disturbance caused by the severe results indicated that some river sections were more suitable spate of 2013 caused a marked reduction in distribution range than others because consistently supported greater sculpin and abundance. In 2014, after the spate, electrofishing surveys densities, being the presence of coarser substrate a significant failed to find the species at several previously recorded sites and factor. Therefore, the causes of the present situation may be it was only present in 40.0% of the sampling sites. Also, mean related, at least in part, to a sub-optimal habitat quality. Main density in 2014 was the lowest of the full period studied. In 2016, habitat alterations in the Garonne drainage are stream population density appeared to start a recovery trend (Fig. 2). channelization and the presence of weirs and dams for The spate also had effects on the size structure, thus, in 2014 hydroelectric purposes. Many channelization projects across

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Spate

1000 70

60

) 800 -1

a 50 h . d

n 600 i

( 40 y t i s

n 30

e 400 d n i Occurrence (%)

p 20 l

u 200 c S 10

0 0 2001-2005 2006-2012 2014 2015 2016

Fig. 2. Mean density (box-plots) and percentage of occurrence (■) of Pyrenean sculpin Cottus hispaniolensis in the sampling sites from 2001 to 2016. Due to unequal sampling effort among years, data is pooled in several time groups. In box-plot, filled circle is the mean and solid horizontal line is the median. Upper and lower box limits are the 25th and 75th percentiles, and bars represent the 5th and 95th percentiles. The spate of June 2013 is represented as a dashed vertical line.

15 2006-2012 Table 2. Multiple linear regression models of mean density and 10 percentage of occurrence of Pyrenean sculpin Cottus hispaniolensis based on habitat and biotic variables (see text). Models were created 5 with stepwise multiple regressions (Adj. = adjusted; RMSE = residual mean square error). The significance level for inclusion of predictor 0 20 40 60 80 100 120 140 160 variables was 0.05. 6 2014 Metric Model Variable Coefficient P 4 Adj. R2 RMSE

2 Density 0.78 0.44 Intercept 8.178 0.0002 h

s <

i Boulders 0.140 0.0001 f 0 f 20 40 60 80 100 120 140 160 Cobble 0.123 0.0006 o

r 8 Sand 0.056 0.0149 e 2015 b

m Presence Intercept

u 0.72 16.30 281.870 0.0003 4 N Boulders 4.412 <0.0001 Cobble 4.581 0.0006 0 Sand 2.178 0.0023 20 40 60 80 100 120 140 160 10 2016 Pyrenean sculpin, i.e. shallow littoral areas (5–20 cm depth) 5 and moderate current velocities (<40 cm s1) with coarse substrate (Legalle et al., 2005a). Although our data did not show significant effects of flow regulation on sculpin density or 0 20 40 60 80 100 120 140 160 occurrence, more research is needed since damming and flow regulation may adversely affect physical and hydraulic habitats, Fig. 3. Length-frequency distributions based on 5 mm FL classes of and therefore could reduce abundance and richness of fish and Pyrenean sculpin Cottus hispaniolensis sampled by electrofishing in macroinvertebrate assemblages (Poff and Zimmerman, 2010). the Spanish part of the Garonne drainage in the 2006–2012 period Management actions that can be taken from the current (n = 74), 2014 (n = 16), 2015 (n = 19) and 2016 (n = 28). analysis to strengthen sculpin populations include: (i) improve the knowledge of biological and ecological traits, together with the drainage have been conducted in the last decades focused the optimal habitat conditions in order to protect and improve on infrastructures and urban areas protection. This type of the habitat quality, (ii) analysis of population genetic data since habitat disturbance reduce the natural streams sinuosity isolation and population bottlenecks may cause additional (Brookes, 1994) and may alter the preferred microhabitat of threats, and (iii) support declining populations with stocking,

Page 4 of 5 R. Rocaspana and E. Aparicio: Knowl. Manag. Aquat. Ecosyst. 2017, 418, 25 either from translocation of wild fish or cultured individuals. In Brookes A. 1994. River channel change. In: Calow P, Petts GE, eds. accordance, a successful pilot project of captive breeding of The Handbook, Vol. 2. Oxford: Blackwell Scientific Pyrenean sculpin was carried out in 2014 at a local fish culture Publications, pp. 55–75. centre. Mature fish (five females and four males) were captured de Sostoa A, Allué R, Bas C, et al. 1990. Peixos (Història Natural dels in early spring from the Garonne River and placed in raceways Països Catalans). Barcelona: Enciclopèdia Catalana, 487 p. (length 120 cm, width 50 cm, and depth 20 cm) with ceramic Doadrio I, Perea S, Garzón-Heydt P, González JL. 2011. Ictiofauna roof tiles distributed on the bottom as shelter. Successful continental española – Bases para su seguimiento. Madrid: spawning occurred at the artificial substrates and ca. 180 Ministerio de Medio Ambiente y Medio Rural y Marino, 610 p. cultured sculpins were released in the wild in October 2014. Freyhof J, Kottelat M, Nolte A. 2005. Taxonomic diversity of However, this action is beginning and further actions are European Cottus with description of eight new species (Teleostei: needed to be implemented. Cottidae). Ichthyol Explor Freshw 16: 107–172. Keith P, Persat H, Feunteun E, Allardi J, coords. 2011. Les poissons Acknowledgments. Financial support was provided by the d’eau douce de France, Biotope Éditions. Paris: Mèze Museum Conselh Generau d’Aran, Fundación Biodiversidad, ENDESA national d’Histoire naturelle, 552 p. and Project LIFE LimnoPirineus (NAT/ES/001210). The Legalle M, Mastrorillo S, Santoul F, Céréghino R. 2005a. Ontogenetic authors are grateful to Ivan Afonso (Biodiversity Service, microhabitat shifts in the bullhead, Cottus gobio L., in a fast Conselh Generau d’Aran), Antoni Palau (University of flowing stream. Int Rev Hydrobiol 90: 310–321. Lleida), Quim Pou-Rovira (Sorelló-LIFE LimnoPirineus) Legalle M, Santoul F, Figuerola J, Mastrorillo S, Céréghino R. 2005b. and Dolors Vinyoles (University of Barcelona) for their Factors influencing the spatial distribution patterns of the bullhead support and collaboration. We also thank Eloi Cruset, Alvaro (Cottus gobio L., Teleostei Cottidae): a multi-scale study. Biodivers Pujals and the squad of forest rangers from the Conselh Conserv 14: 1319–1334. Generau d’Aran, who helped us during field work, Dr. Carles Natsumeda T. 2005. Biotic and abiotic influences on nest-hatching fl Alcaraz and two anonymous referees for valuable comments outcome in the Japanese uvial sculpin Cottus pollux. Environ Biol – on the manuscript. All appropriate ethics and permissions Fish 74: 349 356. required for the realization of this manuscript were obtained, Poff NL, Zimmerman JKH. 2010. Ecological responses to altered fl previously, by the authors. ow regimes: a literature review to inform the science and management of environmental flows. Freshw Biol 55: 194–205. Seber GAF, Le Cren ED. 1967. Estimating population parameters References from catches large relative to the population. J Anim Ecol 36: 631–643. Aparicio E. 2015. First record of a self-sustaining population of Sousa-Santos C, Robalo JI, Pereira A, Doadrio I. 2014. Threatened Alpine charr Salvelinus umbla (Linnaeus. 1758) (, fishes of the world: Cottus hispaniolensis Bacescu-Mester, 1964 ) in Spain. Graellsia 71: e034. (Cottidae). Croatian J Fish 72: 132–133. Aparicio E, Alcaraz C, Carmona-Catot G, et al. 2016. Peixos Tomlinson ML, Perrow MR. 2003. Ecology of the Bullhead. continentals de Catalunya. Ecologia, conservació i guia d’identi- Conserving Natura 2000 Rivers, Ecology Series No. 4. Peter- ficació. Barcelona: Lynx Edicions, 251 p. borough: English Nature, 16 p.

Cite this article as: Rocaspana R, Aparicio E. 2017. Population trends and current status of the endangered Pyrenean sculpin Cottus hispaniolensis in the Spanish part of the Garonne drainage. Knowl. Manag. Aquat. Ecosyst., 418, 25.

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